The relative influence of sea surface temperature anomalies on the benthic composition of an Indo‐Pacific and Caribbean coral reef over the last decade

Abstract Rising ocean temperatures are the primary driver of coral reef declines throughout the tropics. Such declines include reductions in coral cover that facilitate the monopolization of the benthos by other taxa such as macroalgae, resulting in reduced habitat complexity and biodiversity. Long‐term monitoring projects present rare opportunities to assess how sea surface temperature anomalies (SSTAs) influence changes in the benthic composition of coral reefs across distinct locations. Here, using extensively monitored coral reef sites from Honduras (in the Caribbean Sea), and from the Wakatobi National Park located in the center of the coral triangle of Indonesia, we assess the impact of global warming on coral reef benthic compositions over the period 2012–2019. Bayesian generalized linear mixed effect models revealed increases in the sponge, and hard coral coverage through time, while rubble coverage decreased at the Indonesia location. Conversely, the effect of SSTAs did not predict any changes in benthic coverage. At the Honduras location, algae and soft coral coverage increased through time, while hard coral and rock coverage were decreasing. The effects of SSTA at the Honduras location included increased rock coverage, but reduced sponge coverage, indicating disparate responses between both systems under SSTAs. However, redundancy analyses showed intralocation site variability explained the majority of variance in benthic composition over the course of the study period. Our findings show that SSTAs have differentially influenced the benthic composition between the Honduras and the Indonesian coral reefs surveyed in this study. However, the large intralocation variance that explains the benthic composition at both locations indicates that localized processes have a predominant role in explaining benthic composition over the last decade. The sustained monitoring effort is critical for understanding how these reefs will change in their composition as global temperatures continue to rise through the Anthropocene.


| INTRODUC TI ON
Coral reefs harbor the highest levels of biodiversity of all marine ecosystems (Fisher et al., 2015), performing paramount roles in the stability of ocean life (Benkwitt et al., 2020;Oliver et al., 2015). In addition, the extraordinary complexity of coral reefs sustains a range of key ecosystem services to human wellbeing, including food security, storm protection, and economic benefits relevant to hundreds of millions of people around the globe (Foale et al., 2013;Moberg & Folke, 1999;Norström et al., 2016;Woodhead et al., 2019).
However, rising ocean temperatures linked to increased anthropogenic emissions of greenhouse gasses have been identified as a key threat to coral reef persistence (Hughes et al., 2017).
A robust body of evidence has shown that global warming acts as the key driver of coral reef declines throughout the tropics.
Pulse events such as marine heatwaves are widely documented to induce bleaching of corals, a process where photosynthetic endosymbionts are expelled from the cnidarian host (Boilard et al., 2020;Douglas, 2003;Fitt et al., 2001;Suggett & Smith, 2020;Warner et al., 1999). Bleaching is occurring over large spatial scales, resulting in mass mortality of entire coral colonies (Hughes, Anderson, et al., 2018;. Additionally, the continued rise in ocean temperatures is preventing coral reefs from recovering before further pulse events occur (Harrison et al., 2019;Hughes, Anderson, et al., 2018). Rising ocean temperatures also inhibit the recruitment of coral reefs by causing mortality to juvenile corals , highlighting the multifaceted process of coral reef decline via global warming. Thus, global warming will continue to transform coral reefs into taxonomically, physically, and functionally more homogenous environments , reducing biodiversity and impacting ecosystem function (Brandl et al., 2019;Oliver et al., 2015;Pratchett et al., 2011).
As global warming continues to degrade coral reefs across the globe, monopolization by other taxa such as macroalgae where reef corals previously resided can occur rapidly (Bozec et al., 2019;Fulton et al., 2019;Graham et al., 2013;Hughes et al., 2007). Additionally, other taxa may also monopolize space previously inhabited by hard corals, such as sponges (Bell et al., 2013;Lesser & Slattery, 2020;Pawlik et al., 2016) and soft corals (Inoue et al., 2013). Yet these taxa do not provide equal ecological complexity to support biodiversity and provision of ecosystem services as reef-building corals (Friedlander & Parrish, 1998;Hughes et al., 2017;Woodhead et al., 2019). Furthermore, a combination of biotic interactions and abiotic effects can prevent taxa from monopolizing uninhabited space for a period of time, resulting in an increased prevalence of sand or rock across the reef scape, further reducing habitat heterogeneity (Alvarez-Filip et al., 2009). Finally, other nonliving benthic components such as coral rubble can inhabit reef space, a clear indication of hard coral mortality, and thus substratum homogenization. These changes in benthic and taxonomic compositions of coral reefs ultimately represent a phase shifts of coral reefs, which are becoming more common under global warming in the Pacific (Bozec et al., 2019;Ledlie et al., 2007), along the Great Barrier Reef (Hughes et al., 2007) and especially in the Atlantic Ocean (Roff & Mumby, 2012).
Coral reefs in the Wakatobi National Park (WNP) of Indonesia, and Honduras in the Caribbean, represent two extensively monitored locations since 2012, providing an ideal case study for understanding long-term benthic compositional change under sea surface temperature anomalies (SSTAs). In the Honduran reef systems, coral cover has been stable between sites (Titus et al., 2015). Meanwhile, depths between 5 and 15 m are associated with divergent responses between hard coral and macroalgae cover, but not sponge and soft coral cover at Utila, an island north of the Honduras coast (Andradi-Brown et al., 2016). At the Indonesia location, fine-scale site variability has been reported for key benthic components, such as Sponge dominance on the turbid reefs (Biggerstaff et al., 2017;Powell et al., 2014;Rovellini et al., 2019), while algae coverage shows temporal variability across reefs at this location (Marlow et al., 2020). By contrast, hard coral cover has appeared relatively stable at the WNP (Marlow et al., 2020), despite observed general global declines since the turn of the century owing to anthropogenic heating (Bruno & Selig, 2007). However, coral community composition did change in the WNP, with a reduction of ~20% in hard coral cover linked to an intense bleaching event in 2010 (Watt-Pringle et al., 2022).
While previous findings have identified spatial and temporal variations of benthic cover at these extensively monitored locations, the change in benthic composition has not been assessed with satellitederived temperature metrics related to SSTAs, Here we assess the relative role of elevated sea temperatures from remote sensing data for influencing the benthic composition two coral reefs from distinct bioregions from 2012 to 2019.

| Survey locations
Our study aims to compare two major coral reef systems of Honduras and Indonesia (Figure 1) where long-term monitoring by Operation Wallacea has been carried out.
In Honduras, data were collected from multiple reef sites in three distinct locations. Cayos Cochinos Marine Protected Area is a small archipelago close to the Honduran mainland with an extensive network of gently sloping coral reefs and heavily restricted access (Titus et al., 2015). Utila Island is the smallest of the Bay Islands chain and home to a major dive tourism industry and surrounded by a fringing reef ranging from slopes to steeper walls (Andradi-Brown et al., 2016). Finally, Banco Capiro is a recently discovered reef system in the mainland bay of Tela, comprising an offshore bank that is home to an unusually high percentage cover of live coral for the region (Bodmer et al., 2015) and a uniquely high-density population of the keystone herbivorous urchin Diadema antillarum (Bodmer et al., 2021).
The study sites in Indonesia were located in the WNP, Southeast Sulawesi. The park encompasses 1.39 million hectares (https:// wakat obina tiona lpark.id/peta-kerja/) in the center of the Coral Triangle, harboring over 390 species of hard coral, and 590 fish species across the 50 k hectares of coral reefs (Clifton et al., 2010).
Approximately 100 k people reside within the WNP, many of which directly rely on coral reefs for their daily livelihoods (Cullen et al., 2007;Exton et al., 2019).

| Benthic data
Benthic surveys took place during the months of June, July, and  Table 1.

| Environmental data
Heat stress was quantified as SSTAs measured in °C over the last 52 weeks preceding surveying at a 5-km resolution, extracted from Coral Reef Watch (CRW) v3.1 5-km product suite (Liu et al., 2014).
The 5-km daily SSTA product uses the daily climatology (DC) derived from the monthly mean (MM) climatology interpreted from linear interpolation. The MM value is assigned to the 15th day of each corresponding month, where individual days are derived from the linear interpolation. The SSTA value is thus calculated as follows where the SST (sea surface temperature) is the value for the day, and DC is the corresponding DC for that specific day of the year.
The CRW products are highly robust for accurately measuring thermal stress, especially in tropical latitudes (Liu et al., 2014), with many different products utilized for various types of study (e.g., McClanahan et al., 2019McClanahan et al., , 2020. Given the discrepancies in accuracy between satellite-derived temperature data and actual temperature of a given region, small values between −0.2 and +0.2°C are considered climatologically normal for the SSTA product, exemplifying the robustness of CRW data (Liu et al., 2014).
These satellite-derived temperature data are primarily an excellent tool for predicting coral responses to heat stress in shallow water (Johnson et al., 2022a(Johnson et al., , 2022bSully et al., 2019). Additionally, they are also ideal predictors of coral responses of up to 18 m depth for changes in coral assemblages , and coral mortality (Donovan et al., 2021).  such as macroalgae and some sponges (Rovellini et al., 2021), this approach has been successfully employed for assessing coral responses over the time period used (Donovan et al., 2021), which are indicative of coral reef compositional change. Average SSTA values for each location over the course of the previous 52 weeks are summarized in Figure 2. The number of temperature cells used to extract temperature values for the surveys from CRW at each location is in Table 2.

| Statistical analyses
Firstly, a generalized linear model (GLM) with a quasi-Poisson distribution was used to determine whether the average SSTA was increasing through time at each location, as data were Poissondistributed and over-dispersed.

| Bayesian generalized linear models
To assess the response of benthic components to rising ocean temperatures, we used Bayesian GLMs from the "brms" package (Bürkner, 2017), which utilizes the STAN language (Carpenter SSTA were the explanatory effects in the model, run with the random effect of site. Priors were fitted for each model using the "get_ prior" function in the package "brms," which specifies priors for the beta coefficients, intercept, and random of effects of each model (Bürkner, 2017). Models were run for 4000 iterations with 3000 burnins, across four chains. To ensure convergence was achieved trace plots were assessed (Figures S1-S14). Posterior predictive checks were also used to assess model performance ( Figures S1-S14), in addition to each model achieving a Gelman-Rubin statistic (Rhat) of 1 (Bürkner, 2017).

| Ordination analysis
To

| Sea surface temperature anomalies from 2012 to 2019
The average SSTAs over the last decade were highly divergent between the Honduras and Indonesia locations, with peak SSTAs preceding the survey years of 2016 and 2017 for Honduras ( Figure 2).

| Response of benthic components to SSTA over the last decade
Changes in the benthic composition between locations varied from 2012 to 2019 (Figure 3). Thus, as expected, the response of benthic components to SSTAs also varied between locations (Figure 4). Time (year) was a strong predictor of an increase in hard coral cover and sponge cover at the Indonesia location, while also predicting a decrease in coral rubble. At the Honduras location, the time predicted an increase in algae and soft coral cover. However, hard coral cover and rock cover are predicted to decrease through time. Over the last decade, SSTA did not predict any changes in benthic cover at the Indonesia location. Conversely, SSTA predicted an increase in bare rock cover at the Honduras location, while also predicting a reduction in sponge coverage.
Redundancy analysis identified low variance explained by the effects of time (year of survey) and SSTA at Indonesia (5.9%) and Honduras (4.7%) location. However, when adding site in the RDA model ( Figure 5), 69.5% of the variance is explained at Indonesia location while 81.8 is explained at the Honduras location, indicating site variability is the strongest predictor of benthic composition at both these locations.

| Change in the benthic community composition from 2012 to 2019
The   Alvarez-Filip et al., 2009). Meanwhile, the decrease in sponge coverage identified at the Honduras location is convoluted in the literature. Coral loss attributed to global warming leads to an increase in seaweed abundance, which results in an increased production of dissolved organic carbon that is consumed by sponges. Consequently, nutrients released by sponges enhance seaweed abundance, further inhibiting coral cover (Pawlik et al., 2016). Yet, this process is likely constrained in the long term owing to cascading trophic processes (Lesser & Slattery, 2020). Our findings suggest that this increase will not occur at this location under rising sea temperatures. At the Indonesia location, none of the benthic components were predicted to either increase or decrease from the effect of SSTA, suggesting other factors are driving the benthic composition of these reefs.
In contrast to the effects of SSTAs, temporal patterns of variation predicting the benthic composition of reefs at both the Indonesia and Honduras location are prominent. These temporal patterns, which predict compositional changes at the Indonesia location have been previously recorded for sponges, which showed the strongest temporal increase of all the benthic components. This stark increase is most strongly related to the Sampela site where high sedimentation has driven sponge dominance (Biggerstaff et al., 2017).
However, fine-scale temporal variation in sponge and algae coverage on the coral reefs of the WNP are well documented (Marlow et al., 2020;Rovellini et al., 2019), along with interannual variability of algae coverage (Marlow et al., 2020;Rovellini et al., 2021), which are likely overlooked based on our findings (e.g., Figure 3).
The increase in hard corals at the Indonesia location contradicts the assumed temporal stability of hard coral at these reefs ( Colors are from Centropyge loricula using the "fishualize" package (Schiettekatte et al., 2022).

F I G U R E 5
Redundancy analysis of the benthic community composition at each location and their relationship with environmental variables. The left plots are data from Indonesia, while Honduras is shown on the right. The blue text within the plots indicates the individual benthic components (Table 1), while the red text specifies the environmental drivers considered in the model, which includes individual sites. The arrows correspond to the relative influence of environmental variables.
reduction in hard corals from warming and acidification should allow for soft corals to outcompete hard corals (Inoue et al., 2013), which may be occurring at these Honduran reefs.

| Other drivers of reef composition
Given that intrinsic site variability between these two locations appears to be the strongest predictor of benthic composition compared with SSTA and time, it is critical to note other potential drivers of composition at these locations. Firstly, the use of mismatched time series methodology does not capture fine-scale temporal dynamics of species with faster life histories, such as macroalgae and some sponges (Rovellini et al., 2021). These faster life history traits will also influence rock coverage as a bare substrate will be quickly monopolized by these taxa, yet grazing and/or displacement could occur before sampling between years takes place. However, the general effects of using SSTA over the 52-week period have been well validated for coral cover (Donovan et al., 2021), which is the most important component of coral reef complexity. The influence of depth was also not considered within our models owing to the dearth of sufficient data. Yet, coral and algae cover at the Honduras location varies by depth (Andradi-Brown et al., 2016), which is also often assumed to be a refuge for some corals under warming oceans (Bridge et al., 2014). Surveying at both locations encompassed a variety of reef types, zones, and depths, but these data were not specifically recorded during collection so were not included in analyses.
However, for corals specifically, depth certainly does not equal refuge, as temperature sensitivity increases with depth (Bongaerts et al., 2017). Furthermore, at the Honduras location, the impacts of grazing herbivores such as Diadema antillarum, which support ecosystem function by reducing algae coverage, thus facilitating coral cover increase, were not considered as a driver of benthic composition in this study despite their known positive impacts (Bodmer et al., 2015(Bodmer et al., , 2021. Our analysis also did not consider prevailing ocean currents, such as the influence of the Banda and Flores Sea (Gordon et al., 1994), which at the Indonesia location, is hypothesized to provide cooling waters to corals of the WNP, potentially alleviating bleaching during thermal stress. Finally, the lack of information on the level of coral reef species is also not available from monitoring data, which are likely to be an influential factor for assessing changes to the benthic composition under SSTAs. However, data at this resolution on coral reefs are unlikely feasible with citizen science techniques, therefore a trade-off between accuracy and resolution must be considered (Done et al., 2017;Gouraguine et al., 2019).

| CON CLUS ION
In conclusion, our analyses reveal the composition of reefs at both locations has changed over the last decade, with increasing evidence of changes in Honduras during SSTAs compared with the Indonesia location. At the Indonesia location, temporal variation predicts changes in the benthic composition far more than the effect of elevated sea surface temperatures. However, high variance explained of the benthic composition by adding the site to RDA models indicates other fine-scale inter-location factors are likely driving the benthic composition of both these locations. Consequently, continued monitoring of these reefs with a higher taxonomic resolution of data may be beneficial, along with in-situ temperature recordings.
Ultimately, however, the monitoring effort is critical for understanding the local scale composition dynamics of these coral reefs, and how they will change under anthropogenic heating.

ACK N OWLED G M ENTS
JVJ is funded by the Department for Economy (DfE) Northern Ireland. We thank all the volunteers who contribute to the data collection with Operation Wallacea, and Operation Wallacea for sharing their data. We also thank Coral Reef Watch for the maintenance and the open access use of their database. We are grateful to the DfE and Opwall for funding this.

CO N FLI C T O F I NTE R E S T
All authors contributed to the manuscript writing and revisions and declare no conflict of interest.